Skip to main content

Advertisement

SpringerLink
Log in

Occurrence of virulence genes among Vibrio cholerae and Vibrio parahaemolyticus strains from treated wastewaters

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Pathogenic Vibrio species are an important cause of foodborne illnesses. The aim of this study was to describe the occurrence of potentially pathogenic Vibrio species in the final effluents of a wastewater treatment plant and the risk that they may pose to public health. During the 1-year monitoring, a total of 43 Vibrio strains were isolated: 23 Vibrio alginolyticus, 1 Vibrio cholerae, 4 Vibrio vulnificus, and 15 Vibrio parahaemolyticus. The PCR investigation of V. parahaemolyticus and V. cholerae virulence genes (tlh, trh, tdh, toxR, toxS, toxRS, toxT, zot, ctxAB, tcp, ace, vpi, nanH) revealed the presence of some of these genes in a significant number of strains. Intraspecies variability and genetic relationships among the environmental isolates were analyzed by random amplified polymorphic DNA-PCR (RAPD-PCR). We report the results of the first isolation and characterization of an environmental V. cholerae non-O1 non-O139 and of a toxigenic V. parahaemolyticus strain in Tunisia. We suggest that non-pathogenic Vibrio might represent a marine reservoir of virulence genes that can be transmitted between strains by horizontal transfer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmed, A. M., Nakagawa, T., Arakawa, E., Ramamurthy, T., Shinoda, S., & Shimamoto, T. (2004). New aminoglycoside acetyltransferase gene, aac(3)-Id, in a class 1 integron from a multiresistant strain of Vibrio fluvialis isolated from an infant aged 6 months. Journal of Antimicrobial Chemotherapy, 53(6), 947–951.

    Article  CAS  Google Scholar 

  • Alsina, M., & Blanch, A. R. (1994). A set of keys for biochemical identification of environmental Vibrio species. Journal of Applied Bacteriology, 76, 79–85.

    Article  CAS  Google Scholar 

  • Bej, A. K., Patterson, D. P., Brasher, C. W., Vickery, M. C., Jones, D. D., & Kaysner, C. A. (1999). Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh and trh. Journal of Microbiological Methods, 36(3), 215–225.

    Article  CAS  Google Scholar 

  • Brauns, L. A., Hudson, M. C., & Oliver, J. D. (1991). Use of the polymerase chain reaction in detection of culturable and nonculturable Vibrio vulnificus cells. Applied and Environmental Microbiology, 57(9), 2651–2655.

    CAS  Google Scholar 

  • Ceccarelli, D., Salvia, A. M., Sami, J., Cappuccinelli, P., & Colombo, M. M. (2006). New cluster of plasmid-located class 1 integrons in Vibrio cholerae O1 and a dfrA15 cassette-containing integron in Vibrio parahaemolyticus isolated in Angola. Antimicrobial Agents and Chemotherapy, 50(7), 2493–2499. doi:10.1128/AAC.01310-05.

    Article  CAS  Google Scholar 

  • Chen, Y., Johnson, J. A., Pusch, G. D., Morris, J. G., Jr., & Stine, O. C. (2007). The genome of non-O1 Vibrio cholerae NRT36S demonstrates the presence of pathogenic mechanisms that are distinct from those of O1 Vibrio cholerae. Infection and Immunity, 75(5), 2645–2647.

    Article  CAS  Google Scholar 

  • Colombo, M. M., Mastrandrea, S., Santona, A., de Andrade, A. P., Uzzau, S., Rubino, S., & Cappuccinelli, P. (1994). Distribution of the ace, zot, and ctxA Foxin genes in clinical and environmental Vibrio cholerae. Journal of Infectious Diseases, 170(3), 750–751.

    Article  CAS  Google Scholar 

  • Dawyndt, P., Vancanneyt, M., Meyer, H. D., & Swings, J. (2005). Knowledge accumulation and resolution of data inconsistencies during the integration of microbial information sources. IEEE Transactions on Knowledge and Data Engineering, 17, 1111–1126.

    Article  Google Scholar 

  • Di Pinto, A., Ciccarese, G., Tantillo, G., Catalano, D., & Forte, V. T. (2005). A collagenase-targeted multiplex PCR assay for identification of Vibrio alginolyticus, Vibrio cholerae, and Vibrio parahaemolyticus. Journal of Food Protection, 68(1), 150–153.

    Google Scholar 

  • Farina, C., Gnecchi, F., Luzzi, I., & Vailati, F. (2000). Vibrio cholerae O2 as a cause of a skin lesion in a tourist returning from Tunisia. Journal of Travel Medicine, 7(2), 92–94.

    Article  CAS  Google Scholar 

  • Folgosa, E., Mastrandrea, S., Cappuccinelli, P., Uzzau, S., Rappelli, P., Brian, M. J., & Colombo, M. M. (2001). Molecular identification of pathogenicity genes and ERIC types in Vibrio cholerae O1 epidemic strains from Mozambique. Epidemiology and Infection, 127(1), 17–25.

    Article  CAS  Google Scholar 

  • Gil, A. I., Louis, V. R., Rivera, I. N., Lipp, E., Huq, A., Lanata, C. F., Taylor, D. N., Russek-Cohen, E., Choopun, N., Sack, R. B., & Colwell, R. R. (2004). Occurrence and distribution of Vibrio cholerae in the coastal environment of Peru. Environmental Microbiology, 6(7), 699–706.

    Article  Google Scholar 

  • Iyer, L., Vadivelu, J., & Puthucheary, S. D. (2000). Detection of virulence associated genes, haemolysin and protease amongst Vibrio cholerae isolated in Malaysia. Epidemiology and Infection, 125(1), 27–34.

    Article  CAS  Google Scholar 

  • Jermyn, W. S., & Boyd, E. F. (2002). Characterization of a novel Vibrio pathogenicity island (VPI-2) encoding neuraminidase (nanH) among toxigenic Vibrio cholerae isolates. Microbiology, 148(Pt 11), 3681–3693.

    CAS  Google Scholar 

  • Jermyn, W. S., & Boyd, E. F. (2005). Molecular evolution of Vibrio pathogenicity island-2 (VPI-2): mosaic structure among Vibrio cholerae and Vibrio mimicus natural isolates. Microbiology, 151(Pt 1), 311–322.

    Article  CAS  Google Scholar 

  • Khouadja, S., Snoussi, M., Saidi, N., & Bakhrouf, A. (2012). Phenotypic characterization and RAPD fingerprinting of Vibrio parahaemolyticus and Vibrio alginolyticus isolated during Tunisian fish farm outbreaks. Folia microbiologica, 58(3). doi:10.1007/s12223-012-0174-x.

  • Kim, Y. B., Okuda, J., Matsumoto, C., Takahashi, N., Hashimoto, S., & Nishibuchi, M. (1999). Identification of Vibrio parahaemolyticus strains at the species level by PCR targeted to the toxR gene. Journal of Clinical Microbiology, 37(4), 1173–1177.

    CAS  Google Scholar 

  • Koch, W. H., Payne, W. L., Wentz, B. A., & Cebula, T. A. (1993). Rapid polymerase chain reaction method for detection of Vibrio cholerae in foods. Applied and Environmental Microbiology, 59(2), 556–560.

    CAS  Google Scholar 

  • Nandi, B., Nandy, R. K., Mukhopadhyay, S., Nair, G. B., Shimada, T., & Ghose, A. C. (2000). Rapid method for species-specific identification of Vibrio cholerae using primers targeted to the gene of outer membrane protein OmpW. Journal of Clinical Microbiology, 38(11), 4145–4151.

    CAS  Google Scholar 

  • Nishibuchi, M., Janda, J. M., & Ezaki, T. (1996). The thermostable direct hemolysin gene (tdh) of Vibrio hollisae is dissimilar in prevalence to and phylogenetically distant from the tdh genes of other vibrios: implications in the horizontal transfer of the tdh gene. Microbiology and Immunology, 40(1), 59–65.

    Article  CAS  Google Scholar 

  • Okoh, A. I., & Igbinosa, E. O. (2010). Antibiotic susceptibility profiles of some Vibrio strains isolated from wastewater final effluents in a rural community of the Eastern Cape Province of South Africa. BMC Microbiology, 10, 143.

    Article  Google Scholar 

  • Ottaviani, D., Santarelli, S., Bacchiocchi, S., Masini, L., Ghittino, C., & Bacchiocchi, I. (2005). Presence of pathogenic Vibrio parahaemolyticus strains in mussels from the Adriatic Sea, Italy. Food Microbiology, 22, 585–590.

    Article  CAS  Google Scholar 

  • Quindos, G., Salesa, R., Carrillo-Munoz, A. J., Lipperheide, V., Jaudenes, L., San Millan, R., Torres-Rodriguez, J. M., & Ponton, J. (1994). Multicenter evaluation of ATB fungus: a standardized micromethod for yeast susceptibility testing. Chemotherapy, 40(4), 245–251.

    Article  CAS  Google Scholar 

  • Reidl, J., & Klose, K. E. (2002). Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiology Review, 26(2), 125–139.

    Article  CAS  Google Scholar 

  • Ripabelli, G., Sammarco, M. L., McLauchlin, J., & Fanelli, I. (2003). Molecular characterisation and antimicrobial resistance of Vibrio vulnificus and Vibrio alginolyticus isolated from mussels (Mytilus galloprovincialis). Systematic and Applied Microbiology, 26(1), 119–126.

    Article  CAS  Google Scholar 

  • Sechi, L. A., Dupre, I., Deriu, A., Fadda, G., & Zanetti, S. (2000). Distribution of Vibrio cholerae virulence genes among different Vibrio species isolated in Sardinia, Italy. Journal of Applied Microbiology, 88(3), 475–481.

    Article  CAS  Google Scholar 

  • Thompson, C. C., Vicente, A. C., Souza, R. C., Vasconcelos, A. T., Vesth, T., Alves, N., Jr., Ussery, D. W., Iida, T., & Thompson, F. L. (2009). Genomic taxonomy of Vibrios. BMC Evolutionary Biology, 9, 258.

    Article  Google Scholar 

  • Thompson, F. L., Iida, T., & Swings, J. (2004). Biodiversity of vibrios. Microbiology and Molecular Biology Reviews, 68(3), 403–431. table of contents.

    Article  CAS  Google Scholar 

  • WHO. (2002). Cholera, 2001. Weekly Epidemiological Record, 77, 257–268.

    Google Scholar 

  • Zanetti, S., Deriu, A., Volterra, L., Falchi, M. P., Molicotti, P., Fadda, G., & Sechi, L. (2000). Virulence factors in Vibrio alginolyticus strains isolated from aquatic environments. Annali d’Igiene, 12(6), 487–491.

    CAS  Google Scholar 

  • Zhang, X. H., & Austin, B. (2005). Haemolysins in Vibrio species. Journal of Applied Microbiology, 98(5), 1011–1019.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Pr. Mauro M Colombo for assistance with reference strains.

Author information

Authors and Affiliations

  1. Laboratoire d’Analyse, Traitement et Valorisation des Polluants de l’Environnement et des Produits, Département de Microbiologie, Faculté de Pharmacie, Rue Avicenne, 5000, Monastir, Tunisia

    Sadok Khouadja, Besma Baccouche & Amina Bakhrouf

  2. Reparto Adempimenti Comunitari e Sanità Pubblica, Dipartimento di Sanità Pubblica Veterinaria e Sicurezza Alimentare, Istituto Superiore di Sanità, Rome, Italy

    Elisabetta Suffredini & Luciana Croci

Authors
  1. Sadok Khouadja
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisabetta Suffredini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Besma Baccouche
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luciana Croci
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Amina Bakhrouf
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sadok Khouadja.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khouadja, S., Suffredini, E., Baccouche, B. et al. Occurrence of virulence genes among Vibrio cholerae and Vibrio parahaemolyticus strains from treated wastewaters. Environ Monit Assess 186, 6935–6945 (2014). https://doi.org/10.1007/s10661-014-3900-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-014-3900-9

Keywords

Search

Navigation